From Mexico to Michigan and back: An international collaboration investigating primate behavior, ecology, and evolution from multiple perspectives

Evolutionary research benefits form the integration of laboratory and field components to determine factors and processes that affect the evolutionary trajectories of species. Our shared interest in understanding hybridization with genetic admixture as a process that may impact social, behavioral, and ecological features of primates, brought us together in a collaborative project aimed at addressing how vocal variation in two species of howler monkeys in Mexico affects and is affected by hybridization. To achieve this goal, we joined our academic expertise in studying primate genetics, ecology, and behavior under different natural and experimental conditions. We took advantage of decades of experience studying and handing wild howler monkeys for translocation projects to safely sample and study wild populations for this project. Here, we describe the history of our collaboration highlighting how our different perspectives, academic realities, and individual strengths built the foundation for our successful collaboration. We also share our perspectives on how this collaboration opened up new academic venues, broadened our individual perspectives on the integration of different research approaches to address a complex topic, and allowed us to recognize the strength of international collaboration.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/149745/1/ajp22992_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/149745/2/ajp22992.pd

Social correlates of variation in urinary oxytocin concentrations of mantled howler monkeys Alouatta palliata (Gray, 1849) (Primates: Atelidae): A preliminary assessment

There is growing evidence that non-human primate sociality is linked to proximate neuroendocrine mechanisms. Arginine vasopressin, endorphins, and oxytocin may be involved in such mechanisms. Here, we perform a preliminary analysis of the social correlates of variation in urinary oxytocin concentrations in mantled howler monkeys (Alouatta palliata). From January to December 2017, we studied 13 adult mantled howler monkeys belonging to two groups. We recorded the occurrence of social interactions (547.5 observation hours); assessed proximity among group members (2,194 instantaneous recordings); and collected 172 urine samples. Urine samples were assayed (ELISA) for oxytocin concentrations, which were corrected for specific gravity, resulting in 54 analyzed samples. Hormone concentrations increased by approximately 62% when individuals were involved in affiliative interactions. With respect to when no affiliative interactions occurred, urinary oxytocin concentrations were higher when dyads with a low-quality social relationship affiliated. These results agree with previous contentions that this hormone is linked to participation in affiliative interactions. Convergence between these and results from other taxa supports the hypothesis that the biological mechanisms that allow for primate sociality are shared among species.Existe una creciente evidencia de que la sociabilidad en primates no humanos está relacionada con mecanismos neuroendocrinos. La arginina vasopresina, las endorfinas y la oxitocina pueden estar involucradas en tales mecanismos. Aquí, realizamos un análisis preliminar de los correlatos sociales de la variación en las concentraciones de oxitocina urinaria en monos aulladores de manto (Alouatta palliata). De enero a diciembre de 2017, estudiamos 13 monos aulladores de manto adultos pertenecientes a dos grupos. Registramos la ocurrencia de interacciones sociales (547.5 horas de observación); evaluamos la proximidad entre los miembros del grupo (2.194 registros instantáneos); y recolectamos 172 muestras de orina. Analizamos las muestras de orina (ELISA) para determinar las concentraciones de oxitocina, las cuales corregimos por la gravedad específica, lo que resultó en 54 muestras analizadas. Con respecto a cuando no ocurrieron interacciones afiliativas, las concentraciones de oxitocina aumentaron aproximadamente un 62% cuando los individuos participaron en interacciones afiliativas, y las concentraciones de oxitocina fueron mayores cuando díadas con una relación social de baja calidad se afiliaron. Estos resultados convergen con propuestas previas de que la oxitocina está vinculada a la participación en interacciones afiliativas. La convergencia entre estos resultados y los reportados para otros taxa apoya la hipótesis de que los mecanismos biológicos que permiten la sociabilidad de los primates se comparten entre las especies

Isotopic niche partitioning in two sympatric howler monkey species

ObjectivesEcological similarity between species can lead to interspecific trophic competition. However, when ecologically similar species coexist, they may differ in foraging strategies and habitat use, which can lead to niche partitioning. As the body tissues of consumers contain a stable isotope signature that reflects the isotopic composition of their diet, stable isotope analysis is a useful tool to study feeding behavior. We measured the isotopic niche width, which is a proxy for trophic niche width, of mantled (Alouatta palliata) and black (A. pigra) howler monkeys. Specifically, studied populations in allopatry and sympatry to assess whether these species showed niche partitioning.Materials and MethodsBetween 2008 and 2012, we collected hair samples from 200 subjects (113 black and 87 mantled howler monkeys) and used continuous flow isotope ratio mass spectrometry to estimate δ13C and δ15N. We described the isotopic niche width of each species in allopatry and sympatry with the Bayesian estimation of the standard ellipse areas.ResultsIn allopatry, isotopic niche width and isotopic variation were similar in both species. In sympatry, black howler monkeys had a significantly broader isotopic niche, which was mainly determined by high δ15N values, and included the majority of mantled howler monkeys’ isotopic niche. The isotopic niche of mantled howler monkeys did not differ between sympatry and allopatry.ConclusionsThe coexistence of these ecologically similar species may be linked to trophic niche adjustments by one species, although the particular features of such adjustments (e.g., dietary, spatial, or sensory partitioning) remain to be addressed.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/155926/1/ajpa24028.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/155926/2/ajpa24028_am.pd

Alouatta pigra males ignore A. palliata loud calls: A case of failed rival recognition?

ObjectivesWhen closely related species overlap geographically, selection may favor speciesâ specific mate recognition traits to avoid hybridization costs. Conversely, the need to recognize potential sameâ sex rivals may select for lower specificity, creating the possibility that selection in one domain constrains evolution in the other. Despite a wealth of data on mate recognition, studies addressing rival recognition between hybridizing species are limited to a few bird species. Using naïve populations, we examine the extent to which failed rival recognition might have affected hybridization patterns when two species of howler monkeys (Alouatta pigra and A. palliata) first met after diverging in allopatry.MethodsWe simulated first contact between naïve subjects using playback experiments in allopatric populations of the two purebred species. Using linear mixed models, we compared their look, move, and vocal responses to conspecific and heterospecific loud calls.ResultsAlthough not different in overall response strength to playbacks, the two species differed in reaction to heterospecific callers. Male A. pigra ignored calls from male A. palliata, but the reverse was not true.DiscussionDespite striking differences in vocalizations, A. palliata respond equally to calls from both species whereas A. pigra respond only to conspecifics. This apparent failure of A. pigra males to recognize interspecific rivals might have biased hybridization (F1 hybridsâ =â male A. palliata x female A. pigra), a pattern previously hypothesized based on genetic analysis of hybrids. Given that A. pigra males could be losing reproductive opportunities to heterospecific males, our findings add to growing evidence of potential costs for overly specific species recognition.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/144221/1/ajpa23443.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/144221/2/ajpa23443_am.pd

Digestive strategies and food choice in mantled howler monkeys Alouatta palliata mexicana : Bases of their dietary flexibility

Mantled howler monkeys (Alouatta palliata) occupy a wide variety of tropical habitats and are the most folivorous of New World primates. However, their diet may include fruits, buds, petioles, and flowers, as well as leaves, suggesting they must cope wit

Effect of ancestry on behavioral variation in two species of howler monkeys ( Alouatta pigra and A. palliata ) and their hybrids

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/108292/1/ajp22273.pd

Primates living outside protected habitats are more stressed: the case of black howler monkeys in the Yucatán Peninsula.

The non-invasive monitoring of glucocorticoid hormones allows for the assessment of the physiological effects of anthropogenic disturbances on wildlife. Variation in glucocorticoid levels of the same species between protected and unprotect areas seldom has been measured, and the available evidence suggests that this relationship may depend on species-specific habitat requirements and biology. In the present study we focused on black howler monkeys (Alouatta pigra), a canopy-dwelling primate species, as a case study to evaluate the physiological consequences of living in unprotected areas, and relate them with intragroup competition and competition with extragroup individuals. From February 2006 to September 2007 we collected 371 fecal samples from 21 adults belonging to five groups (two from protected and three from unprotected areas) in Campeche, Mexico. We recorded agonistic interactions within groups and encounters with other groups (1,200 h of behavioral observations), and determined fecal glucocorticoid metabolite (FGM) concentrations with radioimmunoassays. We used linear mixed models and Akaike's information criterion to choose the best model explaining variation in FGM concentrations between protected and unprotected areas calculated from five categorical variables: habitat type (protected vs. unprotected), participation in agonistic interactions, intergroup encounters, sex and female reproductive state, and season. The best model included habitat type, the interaction between habitat type and agonism, and the interaction between habitat type and season. FGM concentrations were higher in unprotected habitats, particularly when individuals were involved in agonistic interactions; seasonal variation in FGM concentrations was only detected in protected habitats. High FGM concentrations in black howler monkeys living in unprotected habitats are associated with increased within-group food competition and probably associated with exposure to anthropogenic stressors and overall food scarcity. Because persistent high GC levels can be detrimental to health and fitness, populations living in disturbed unprotected areas may not be viable in the long-term

Howler Monkeys (Alouatta palliata mexicana) Produce Tannin-Binding Salivary Proteins

Dietary tannins are ubiquitous in woody plants and may have serious negative effects on herbivores by inducing a loss of dietary protein and producing toxins if they are hydrolyzed in the gut. Many herbivorous mammals counter the negative effects of tannins through tannin-binding salivary proteins (TBSPs) that inactivate tannins by forming insoluble complexes and prevent them from interacting with other more valuable proteins. Howlers are the most folivorous New World primates and ingest foods with varying tannin content. We studied the presence of TBSPs in six wild mantled howlers (Alouatta palliata mexicana) immediately after capture and in captivity when fed on two diets composed of natural ingredients: a mixture of fruit and leaves or only leaves. Protein concentration was determined in whole saliva samples, followed by gel electrophoresis. We identified two protein bands of 17 and 25 kDa that have tannin-binding capacity. Although the monkeys ate almost twice as much condensed tannins in the leaf diet than in the fruits and leaves diet (7 vs. 4 g/d dry matter) the salivary protein concentration did not differ between the two diets (leaf diet: 3.29 ± SE 0.82 vs. fruit and leaves diet: 3.42 ± SE 0.62 mg/ml) and we found no additional protein bands in response to either diet. We suggest that the continuous expression of TBSPs is part of a dietary strategy that enables howlers to consume diets with variable tannin contents, thus partly explaining their dietary flexibility. Although the importance of salivary proteins to arboreal primates is broadly accepted, to our knowledge this is the first report of TBSPs in any Neotropical primate

Mean (± SE) rates of within-group agonistic interactions and encounters with extragroup individuals for groups of black howler monkeys in unprotected and protected areas in Campeche, Mexico.

<p>Mean (± SE) rates of within-group agonistic interactions and encounters with extragroup individuals for groups of black howler monkeys in unprotected and protected areas in Campeche, Mexico.</p

Characteristics of the groups and habitats of black howler monkeys that were studied in unprotected and protected areas in Campeche, Mexico.

<p>*Calculated as mean number of individuals during the two sampling periods (i.e., rainy and dry season).</p><p>Characteristics of the groups and habitats of black howler monkeys that were studied in unprotected and protected areas in Campeche, Mexico.</p